Ion and metabolite transport in the chloroplast of algae: lessons from land plants

Abstract

Chloroplasts are endosymbiotic organelles and play crucial roles in energy supply and metabolism of eukaryotic photosynthetic organisms (algae and land plants). They harbor channels and transporters in the envelope and thylakoid membranes, mediating the exchange of ions and metabolites with the cytosol and the chloroplast stroma and between the different chloroplast subcompartments. In secondarily evolved algae, three or four envelope membranes surround the chloroplast, making more complex the exchange of ions and metabolites. Despite the importance of transport proteins for the optimal functioning of the chloroplast in algae, and that many land plant homologues have been predicted, experimental evidence and molecular characterization are missing in most cases. Here, we provide an overview of the current knowledge about ion and metabolite transport in the chloroplast from algae. The main aspects reviewed are localization and activity of the transport proteins from algae and/or of homologues from other organisms including land plants. Most chloroplast transporters were identified in the green alga Chlamydomonas reinhardtii, reside in the envelope and participate in carbon acquisition and metabolism. Only a few identified algal transporters are located in the thylakoid membrane and play role in ion transport. The presence of genes for putative transporters in green algae, red algae, diatoms, glaucophytes and cryptophytes is discussed, and roles in the chloroplast are suggested. A deep knowledge in this field is required because algae represent a potential source of biomass and valuable metabolites for industry, medicine and agriculture.

Keywords: Algae; Channel; Chloroplast; Metabolism; Photosynthesis; Transporter.

Fig. 1

Schematic view of plastid evolution in the history of photosynthetic eukaryotes. The engulfment of a cyanobacterium by a primitive eukaryotic host (primary endosymbiosis) gave rise to three algal lineages: Chlorophyta, Rhodophyta and Glaucophyta. The green lineage Streptophyta evolved from Chlorophyta. The engulfment of green and red algae by different hosts (secondary endosymbiosis) resulted in the green lineages Euglenophyta and Chlorarachniophyta and in the red lineage Chromalveolata, that is further divided into four major subgroups, namely Heterokontophyta, Cryptophyta, Haptophyta and Alveolata. Primary plastids are surrounded by two membranes, whereas three or four membranes can be present in the secondary plastids. The figure is a modified version of Fig. 1 from Facchinelli and Weber [30] (reproduced with permission from the authors)

Fig. 2

Algal models. Data mining in ‘all databases’ of the Web of Science using ‘algal genus’ (a–c) or ‘algal genus and transporter’ (d) as keywords in titles of publications. The data revealed three categories, namely historical, recent and emerging models (see the text for details). The most used models for transporter studies belong to the green algae and include Chlamydomonas. The colors used to represent various algal groups were green (green algae), red (red algae), brown (diatoms), magenta (eustigmatophytes), blue (alveolates) and yellow (haptophytes)

Fig. 3

Ion and metabolite transport proteins of the chloroplast envelope and thylakoid membrane from algae. Proteins identified or characterized in at least one algal model are framed with continuous line. Plant homologues genes coding for putative transporters in algae are framed with broken lines. Green algae, red algae and diatoms are represented in green, red and brown, respectively